Smooth Muscle Mechanically Sculpts the Airway Epithelium in Birds and Reptiles

The reptilian lung, with its basic sac-like structure, is considered to be the most evolutionarily basic among amniotes. In comparison, mammalian and avian lungs are much more complex and finely branched. Smooth muscle (SM) is required for branching in the early mouse lung but to date this tissue remains uninvestigated in other amniotes. The respiratory system of birds contains a network of connected airways that begin as terminal structures but fuse as embryonic development progresses. We found that prior to airway fusion in the domestic chicken, Gallus gallus, the airways initiate branches in the direction of their target, which will make the first contact. These new branches occur in regions devoid of SM, implying a role for it in shaping the airway epithelium prior to fusion. We have also examined early development of reptile lungs using the brown anole, Anolis sagrei, as a model organism and found that SM is present in a mesh-like arrangement and regulated by the same signaling pathways as in the murine lung. Contraction of SM defines the shape of the epithelium. Despite the fact that the tissue forms at different periods in development and in varying patterns, these data suggest an evolutionarily conserved mechanism for SM as a physical force in airway morphogenesis.